An H3K27me3 demethylase-HSFA2 regulatory loop orchestrates transgenerational thermomemory in Arabidopsis

First author: Junzhong Liu; Affiliations: CAS Center for Excellence in Molecular Plant Sciences (中科院分子植物科学卓越创新中心): Shanghai, China

Corresponding author: Zuhua He 

Global warming has profound effects on plant growth and fitness. Plants have evolved sophisticated epigenetic machinery to respond quickly to heat, and exhibit transgenerational memory of the heat-induced release of post-transcriptional gene silencing (PTGS). However, how thermomemory is transmitted to progeny and the physiological relevance are elusive. Here we show that heat-induced HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) directly activates the H3K27me3 demethylase RELATIVE OF EARLY FLOWERING 6 (REF6), which in turn derepresses HSFA2. REF6 and HSFA2 establish a heritable feedback loop, and activate an E3 ubiquitin ligase, SUPPRESSOR OF GENE SILENCING 3 (SGS3)-INTERACTING PROTEIN 1 (SGIP1). SGIP1-mediated SGS3 degradation leads to inhibited biosynthesis of trans-acting siRNA (tasiRNA). The REF6-HSFA2 loop and reduced tasiRNA converge to release HEAT-INDUCED TAS1 TARGET 5 (HTT5), which drives early flowering but attenuates immunity. Thus, heat induces transmitted phenotypes via a coordinated epigenetic network involving histone demethylases, transcription factors, and tasiRNAs, ensuring reproductive success and transgenerational stress adaptation.

全球变暖对于植物的生长和适应产生了深远的影响。植物演化出了精细的表观机制来快速响应高温，并且高温诱导的转录后基因沉默PTGS能够跨代遗传。然而，植物对于温度记忆是如何遗传给子代的，以及其生理学基础还不清楚。本文的研究显示高温诱导的热休克转录因子HSFA2直接激活H3K27me3去甲基化酶REF6，进而反过来解除HSFA2的抑制。REF6和HSFA2一道建立起了一个可遗传的反馈回路，激活E3泛素连接酶SGS3-SGIP1。SGIP1介导的SGS3降解导致tasiRNA的生物合成受到抑制。REF6-HSFA2循环以及tasiRNA覆盖度的减少都有助于HTT5基因的激活，HTT5能够驱动植株进入早花，但同时会牺牲植株的自身免疫。因此，高温通过一个涉及到组蛋白去甲基化、转录因子以及tasiRNAs等相互协作的表观网络来确保植株成功生殖和子代的胁迫适应，进而实现表型的跨代遗传。

通讯：何祖华 (http://sourcedb.sibs.cas.cn/zw/rck/200906/t20090629_1856172.html)

个人简介：1993-1996年，浙江大学生物技术研究所，植物分子生物学和植物病理学博士；1997-1998年，美国加州Salk研究所，植物细胞和分子生物学博士后； 1999-2000年，加州大学Davis分校，植物病理系博士后。

研究方向：植物抗病信号转导、功能基因和信号途径互作。

doi: https://doi.org/10.1038/s41422-019-0145-8

Journal: Cell Research

Published date: February 18, 2019